The Role of Plantigrady and Heel-Strike in the Mechanics and Energetics of Human Walking with Implications for the Evolution of the Human Foot James T

Home , Digitigrade, Heel, Plantigrade

RESEARCH ARTICLE The role of plantigrady and heel-strike in the mechanics and energetics of human walking with implications for the evolution of the human foot James T. Webber* and David A. Raichlen

ABSTRACT mid- or forefoot contact. Given the importance of limb length to Human bipedal locomotion is characterized by a habitual heel-strike cursorial mammals, it is uncertain why humans use a plantigrade (HS) plantigrade gait, yet the significance of walking foot-posture is foot posture with a consistent HS during walking (Cunningham not well understood. To date, researchers have not fully investigated et al., 2010). the costs of non-heel-strike (NHS) walking. Therefore, we examined A popular hypothesis is that the human HS gait evolved to reduce walking speed, walk-to-run transition speed, estimated locomotor the energy costs of walking (Cunningham et al., 2010; Usherwood costs (lower limb muscle volume activated during walking), impact et al., 2012). This hypothesis is supported by studies showing transient (rapid increase in ground force at touchdown) and effective subjects had relatively high energy costs of locomotion (COL) when limb length (ELL) in subjects (n=14) who walked at self-selected asked to walk with digitigrade foot postures compared with typical speeds using HS and NHS gaits. HS walking increases ELL plantigrade HS walking (Cunningham et al., 2010). Yet, human compared with NHS walking since the center of pressure translates lower limb anatomy is not adapted for full digitigrady and it is anteriorly from heel touchdown to toe-off. NHS gaits led to decreased possible that these experiments captured the energetic costs of novel absolute walking speeds (P=0.012) and walk-to-run transition speeds gaits. Non-human apes may offer more context into how and why (P=0.0025), and increased estimated locomotor energy costs habitual HS walking evolved in humans because we often assume (P<0.0001) compared with HS gaits. These differences lost that traits shared among apes may have been present in our pre- significance after using the dynamic similarity hypothesis to bipedal ancestors. Extant non-human apes use an array of account for the effects of foot landing posture on ELL. Thus, plantigrade walking gaits, some of which lack consistent heel reduced locomotor costs and increased maximum walking speeds strikes (Schmitt and Larson, 1995). For example, researchers have in HS gaits are linked to the increased ELL compared with NHS shown that our closest living relatives, bonobos (Pan paniscus) and gaits. However, HS walking significantly increases impact transient common chimpanzees (Pan troglodytes), use a wide range of values at all speeds (P<0.0001). These trade-offs may be key to landing postures, from a traditional human-like heel strike, to understanding the functional benefits of HS walking. Given the landings where the heel does not touch down until the second half of current debate over the locomotor mechanics of early hominins and stance phase (see Elftman and Manter, 1935; Vereecke et al., 2003). the range of foot landing postures used by nonhuman apes, we Most often, these apes use gaits where the heel and mid-foot contact suggest the consistent use of HS gaits provides key locomotor the ground simultaneously, which also differ from human HS advantages to striding bipeds and may have appeared early in walking where initial ground contact is made by the heel alone hominin evolution. (Elftman and Manter, 1935; Vereecke et al., 2003). Thus, the key human evolutionary shift from the non-hominin ape foot landings KEY WORDS: Bipedalism, Heel-strike, Limb length, Locomotion, appears to be the consistent use of heel-only landing postures. Australopithecus sediba, Homo floresiensis The goal of this study is to better understand the advantages and disadvantages of this shift to consistent HS gaits. To accomplish this INTRODUCTION goal, we measured the mechanics and energetics of human walking Plantigrady is rare among cursorial mammals (Hildebrand and with the two footfall extremes seen in ape-like plantigrade walking: Goslow, 1998), which typically utilize digitigrade or unguligrade an HS, where touchdown occurs with the heel only, and a non-heel gaits to maximize limb length, which is a key determinant of the strike (NHS), where initial ground contact occurs at mid-foot and energetic cost of locomotion (Hildebrand and Goslow, 1998; Kram the heel lands later in stance. Interestingly, although humans do not and Taylor, 1990; Pontzer, 2007a). Humans represent an exception habitually walk with either digitigrade or more ape-like gaits, to this pattern (Cunningham et al., 2010) as we possess adaptations Lieberman et al. (2010) found that many individuals adopt NHS for endurance terrestrial running (Bramble and Lieberman, 2004; gaits at running speeds, similar to those used at times by nonhuman Carrier, 1984), combined with plantigrade feet and a prominent heel apes. Running with an HS foot posture produces rapid and strike (HS), during walking gaits, where the foot touches down heel potentially dangerous increases in the ground reaction force first on the calcaneal tuberosity in a dorsiflexed posture, without (GRF), known as an impact transient (IT), just after the heel impacts the ground (Lieberman et al., 2010). NHS footfalls seem to School of Anthropology, University of Arizona, Tucson, AZ 85721, USA. benefit runners by reducing ITs at higher locomotor speeds (Lieberman et al., 2010), possibly decreasing injury rates *Author for correspondence ([email protected]) (Lieberman, 2012) without increasing locomotor costs (Divert J.T.W., 0000-0002-5354-9457 et al., 2005, 2008; Franz et al., 2012; Kram and Franz, 2012). By specifically exploring the possible benefits of using an HS at slow

Received 5 February 2016; Accepted 18 September 2016 locomotor speeds, we hope to better understand why a consistent Journal of Experimental Biology

3729 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610

A List of symbols and abbreviations COL cost of locomotion COP center of pressure

COPc change in center of pressure (m) DC dynamically calculated DSH dynamic similarity hypothesis _ 3 −1 NHS ECOL estimated cost of locomotion (cm Ns ) HS ELL effective limb length (m)

Fmusc muscle force Fr Froude number Fr′ plantigrade adjusted Froude number GRF ground reaction force (N) B C

HS heel-strike COPc IT impact transient d d 1 2 lfasc muscle fascicle length L limb length (m) L′ plantigrade adjusted limb length (m) θ θ M moment 1 2 NHS non-heel-strike tc foot contact time (s) LЈ 3 −1 Vmusc volume of active muscle (cm N ) WTR walk-to-run

HS evolved in our bipedal ancestors, and whether NHS gaits offer any advantages that may explan their occasional use in other apes. Fig. 1. Differences in posture and limb length in heel-strike (HS) and non- heel-strike (NHS) gaits. (A) Examples of foot posture at initial touchdown, HS Plantigrade walking and effective limb length and NHS. Dashed line indicates surface. (B) Depiction of L′, effective limb As noted by Cunningham et al. (2010), human use of plantigrade length (m), modeled as a point mass on the end of a rigid limb, taking into foot postures is unique among organisms adapted for long distance consideration COPc, the translation in COP during stance and hip excursion angle θ. (C) Depiction of L′ added limb length (region circled in B), see travel since plantigrady reduces hindlimb length compared with Materials and methods for details. digitigrade postures. Limb length is a key determinant of walking mechanics and energetics because when modeled as an inverted pendulum, the limb acts as a strut during stance phase, with the humans, many of the foot postures used by nonhuman apes lead to center of mass vaulting over the point of ground contact (Alexander, reduced total translation of the COP (Vereecke et al., 2003). For 1976; Gray, 1944; Kuo, 2001; Pontzer, 2005). Long limbs reduce example, when bonobos land on both the heel and midfoot energy costs in this model by increasing step lengths, which leads to simultaneously (Elftman and Manter, 1935; Vereecke et al., 2003, longer time periods for accelerating the center of mass and reduced 2005), the COP originates between the heel and forefoot, rather than rates of force generation (Pontzer, 2007a). directly under the heel. Therefore, a consistent HS landing posture Characterizing the effects of plantigrade HS walking on the that maximizes COP translation may be a novel evolutionary length of the pendulum strut may help to explain why this footfall solution to lengthening inverted pendulum struts from an ape-like pattern evolved. Researchers typically use either a linear sum of ancestral condition. skeletal elements (Steudel and Beattie, 1995), the height of the hip We use the dynamic similarity hypothesis (DSH) to test this in quiet stance (Pontzer, 2007a) or hip height at mid-stance during model of inverted pendulum strut length. The DSH suggests that locomotion to describe effective limb length (ELL: average length the motions of two animals are comparable if they can be made of the strut over a step). These lengths assume the pivot point of the similar through dimensional scaling (Alexander and Jayes, 1983). inverted pendulum is fixed at ground contact and therefore Dimensionless parameters can be compared at speeds where the plantigrady should reduce ELL compared with digitigrade foot ratios of inertial to gravitational forces acting on two moving postures. However, the pivot point translates anteriorly during a step systems are equal. This condition is met when organisms walk at the [i.e. the center of pressure (COP) shifts continuously throughout the same Froude number (Fr; Alexander, 1989): stance phase] in plantigrade walkers. Pontzer (2007b) suggested that v2 a significant anterior shift in the COP throughout the step (COPc; Fr ¼ ; ð1Þ see Fig. 1) may actually increase the ELL because the pivot point of gL the inverted pendulum strut would occur significantly below the foot (see Fig. 1B; Pontzer, 2007b). Additionally, Pontzer (2007b) where v is velocity (m s−1), g is gravitational acceleration showed that an estimate of ELL that took COP translation into (9.81 m s−2) and L is a characteristic length. Most researchers account (L′) was a significantly better predictor of the force required assume hip height represents the length of the pendulum strut when to accelerate the center of mass during walking than hip height alone applying the DSH to animal locomotion. However, if Pontzer’s in humans. (2007b) analysis is correct, researchers should instead use the length Based on this view of ELL, an HS walking gait with a plantigrade of the strut calculated from the true pivot point of the inverted foot may significantly increase the length of an inverted pendulum pendulum (L′). In this study we use both L and L′ in calculations of strut, even if this foot posture reduces hip height from the ground in Fr to compare HS and NHS human walking movements in the same quiet stance. Compared with the consistent use of an HS gait in subjects. This analysis will help us to determine whether differences Journal of Experimental Biology

3730 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610 in mechanics and energetics between these gaits are due primarily to with heel contact occurring later in the step (see Fig. 2B). This foot differences in the length of the inverted pendulum strut. If this posture was demonstrated to the subjects after a verbal explanation. hypothesis is supported, mechanical differences between footfall Subjects performed practice trial walks to adjust to this change in gait patterns found when calculating Fr using L should disappear when before data collection began. As with the HS trials, subjects were subjects walk at comparable Fr numbers calculated with L′. instructed to walk at self-selected, preferred (1.01±0.20 m s−1), slow Here, we examine two potential benefits of HS walking and one (0.78±0.19 m s−1) and fast (1.31±0.21 m s−1) speeds. potential cost using this dynamic similarity analysis. First, since Kinematic data were collected at 200 Hz using a Vicon high- previous work suggests that ELL is a main determinant of the costs speed, six-camera, motion capture system (Hauppauge, NY). of locomotion (as described above, see Kram and Taylor, 1990; Twenty-four reflective markers were affixed to the subjects at Pontzer, 2007b), we determined the effects of HS and NHS walking joint centers, limb segments, and foot landmarks including the first on estimates of the energy costs of locomotion. Second, we and fifth distal metatarsal heads, lateral ankle, and heel. An AMTI measured the effects of foot-contact posture on the walk-to-run multi-axis force plate (Watertown, MA) embedded midway along (WTR) transition speed. Changes in ELL should affect WTR the track collected kinetic data at 4 kHz. A successful trial required transitions because bipeds transition to running gaits at dynamically complete, single-foot contact with the force plate using the specified similar speeds, dependent largely on limb length and gravity (Kram foot-strike. Trial data were averaged at each speed and foot-posture et al., 1997; Raichlen, 2008; Usherwood, 2005). Finally, we explore before data analysis. the possibility that NHS gaits may reduce ITs at walking speeds, L was calculated from the average hip height (m) throughout a step similar to the effects of NHS gaits on ITs at running speeds (see following Pontzer (2007b). L′ was calculated two ways. First, Lieberman et al., 2010). following Pontzer (2007b), L′ was calculated trigonometrically at touchdown and toe-off using the distance in meters the COP traveled MATERIALS AND METHODS in the sagittal plane (between touchdown and toe-off) and hip Subjects excursion angle (see Fig. 1C). The two limb lengths obtained from Fourteen adults (7 men and 7 women) with a mean age of 23.7± touchdown and toe-off were averaged to produce an L′ during stance. 4.4 years and body mass of 69.2±16.6 kg took part in this study. All Second, L′ was calculated dynamically as the distance between the subjects were healthy and free of injury at the time of the study. In hip and the average intersection point for all hip-to-COP vectors for order to avoid confounding variables, dancers and individuals with each motion analysis frame of the step. Dynamically calculated (DC) experience running barefoot or in minimalist shoes were not L′ was calculated as the average intersection point between all hip-to- selected to participate in this study. Subjects performed all tasks COP vectors throughout the step. Kinetic data at 4 kHz were barefoot. Prior to starting, the details of the study were explained to resampled to match the kinematic data collected at 200 Hz. For every all participants and informed consent (approved by the University of frame (200 frames s−1), a vector from the greater trochanter marker to Arizona Institutional Review Board) was provided. the center of pressure was calculated in the sagittal plane. The intersections (pivot of the strut for the inverted pendulum between Foot posture kinematic and kinetic data collection any two points) of all combinations of vectors were calculated and The study consisted of two separate experimental activities. The first then averaged. Limb length was then calculated for each frame of the task involved walking along a 4 m trackway across a range of speeds step from the hip joint marker to the average pivot point in the sagittal under two conditions: (1) landing with a HS (see Fig. 2A), and (2) plane. While values were similar between subjects, dynamically landing with a NHS foot posture at initial contact (see Fig. 2B; circles calculated limb lengths were significantly longer than those highlight estimated COP translation shortly after touchdown). calculated from touchdown and toe-off only (P<0.001). However, Subjects were first instructed to walk (HS) at their self-selected, as noted below, results of locomotor comparisons between HS and preferred walking speed for 5 trials (1.14±0.15 m s−1). The same NHS gaits do not change when using either the two-point method or procedure was followed for a slow self-selected walking speed the dynamic method. This method provided similar results to the (0.78±0.18 m s−1) and a fast self-selected walking speed (1.47± method introduced by Pontzer (2007b; see Fig. S3 for results using 0.21 m s−1). After the first three conditions were met, subjects were the second, DC method). directed to walk with a NHS gait, contacting the ground with the distal metatarsal heads (balls of the foot) initially instead of the heel, Active muscle volume and estimated cost of locomotion The energy cost of activating muscle to support the body was used _ as an estimation of the metabolic cost of locomotion (ECOL) following validation by numerous studies across a range of species, including bipedal birds, quadrupedal mammals, and humans (Biewener et al., 2004; Foster et al., 2013; Griffin et al., 2004; A Kram and Taylor, 1990; Pontzer, 2005, 2007b, 2009; Roberts et al., 1998a,b; Sockol et al., 2007; Taylor, 1994; Wright and Weyand, 2001). Inverse dynamics (performed in MATLAB, MathWorks) was used to estimate the change in muscle force production due to _ −1 differences in foot-posture. ECOL (J N s ) is calculated as:

_ Vmusc ECOL ¼ k, ð2Þ B tc

3 −1 −1 Fig. 2. HS and NHS plantigrady. Differences in COP translation in HS (A) and where Vmusc (cm N ) is active muscle volume, tc (s ) is the time − NHS (B) plantigrady occurring after foot touchdown. Circled regions indicate the foot is in contact with the ground and k (J cm 3) is a constant that the estimated COP. determines the rate at which a unit volume of muscle uses energy Journal of Experimental Biology

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(Roberts et al., 1998b). Since k is a constant at most walking speeds programmed treadmill function, which began at a speed of (Griffin et al., 2004; Roberts et al., 1998b), it was excluded from our 1.52 m s−1 and increased by 0.089 m s−1 every 30 s. The _ calculation of ECOL. transition speed was recorded only when subjects ran a complete Vmusc is the product of muscle fascicle length (lfasc, cm), and the 30 s interval, giving them time to switch back to walking if running cross sectional area (A,cm2) of activated muscle (Pontzer et al., 2009; at the speed felt awkward to ensure a complete transition to running. Sockol et al., 2007). Here, average muscle group lfasc was calculated The test was then stopped and the subjects went back to walking at following Biewener et al. (2004) and scaled to body mass for subjects 1.33 m s−1 for a 5 min cool down. Subjects then repeated the WTR in this study. A is proportional to the muscle force (Fmusc) produced trial using an NHS gait. For the second WTR trial, subjects were during walking and is calculated as the muscle force (N) required to asked to walk with the same forefoot gait used in the motion capture extend the limb in response to flexion moments (M) at a specific walkway trials. joint, and the constant σ (where σ is muscle force per unit cross- sectional area, N cm−2) (Biewener et al., 2004). To estimate costs Data analysis across experimental conditions, we assume σ remains constant To determine whether the effects of HS on walking mechanics and despite differences in joint angles during stance phase when walking energetics are due mainly to increased ELL (see Fig. 1), we with an HS and NHS gaits. This assumption is supported by previous compared locomotor variables at Froude numbers calculated with studies that have used this model to successfully predict energy costs hip height (L), and L′. Fr using L, and Fr′ using L′, were calculated in humans and other mammals walking and running with different and compared for each motion capture trial between each self- limb joint postures (Foster et al., 2013; Ren et al., 2010; Sockol et al., selected speed category (slow, preferred and fast) for both foot 2007; Wright and Weyand, 2001). postures to examine the role of ELL in determining the energy costs Fmusc is determined by calculating external moments (M) acting and speed of walking. at each joint (Biewener et al., 2004). Moments were calculated using Between-subject and between-speed differences were tested for GRF vectors, limb segment accelerations, and flexion moments Fr, Fr′, L, and L′ with a repeated-measures two-way analysis of arising from two-joint muscles (Biewener et al., 2004; Winter, variance (ANOVA) test, using foot-posture and self-selected speed 2009). The finite differences method was used to calculate category (as multiple conditions). The relationship between Fr, Fr′ _ segmental acceleration (Winter, 2009), and limb segment inertial and ECOL, and Fr′ and IT, were tested using linear mixed-effects properties were estimated following Winter (2009). Net moments analyses with Fr or Fr′, foot posture (HS versus NHS) and IT as fixed were calculated at each lower limb joint using the free-body method effects, and subject as a random effect having an interaction with foot (Winter, 2009). The extensor muscle forces at each joint (hip, knee, posture. Associated P-values were found by likelihood ratio tests of and ankle) balancing these moments were calculated following the full model versus the model without the effects in question. The equations in Biewener et al. (2004): WTR transition speed was compared between HS and NHS trials with a Student’s t-test. For all tests, level of significance was 0.05. Mankle ¼ Fankle rankle; ð3Þ

Mknee¼ Fknee rknee FðGÞknee rðGÞknee FðHÞknee rðHÞknee; ð4Þ RESULTS Effective limb length and dynamic similarity M ¼ F r Fð Þ rð Þ ; ð5Þ hip hip hip RF hip RF hip We hypothesized that NHS walking would lead to a shorter L′, where G (gastrocnemius), H (hamstrings) and RF (rectus femoris) forcing subjects to walk at lower absolute speeds. Indeed, L′ was are muscles acting on two joints and forces are calculated assuming significantly shorter in NHS trials (Fig. 3; −0.185±0.029 m, the force produced by each is proportional to their physiological F1,13=459.8, P<0.0001). Additionally, human HS plantigrade gaits cross-sectional area (Biewener et al., 2004). Human anatomical increased L′ significantly more than adding the utilized length of the moment arms were calculated from equations that relate moment foot to the hindlimb, as in a digitigrade gait (the limb length gained arms to joint angles (Németh and Ohlsén, 1985; Rugg et al., 1990; by the translating pivot point was 24.19±7.16% higher than the sum Visser et al., 1990) and scaled to segment length. Relating moment of foot length and hip height, P<0.0001). This estimate is likely to be arms to joint angles allows for an estimation of anatomical moments rmusc, while joint angles change during locomotion. Finally, following Biewener et al. (2004), muscle force impulses were 1.4 * divided by the GRF impulse to calculate the total volume of active muscle for use in Eqn 2: 1.3 Ð Ð Ð l ð Þ F þ l ð Þ F þ l ð Þ F V ¼ fasc hip hip fasc kneeÐ knee fasc ankle ankle : 1.2 musc GRF s ð6Þ 1.1 ELL (m) ELL 1 Treadmill walk-to-run speed determination Subjects were also asked to participate in two separate WTR speed determination procedures, which were modified from Farinatti and 0.9 Monteiro (2010). Initially, subjects became accustomed to walking on a treadmill (SOLE Fitness, Salt Lake City, UT) with a 5 min 0.8 warm up. The warm-up consisted of a non-recorded walk at a speed HS LЈ NHS LЈ −1 of 1.33 m s . Once subjects completed the warm up, a covering Fig. 3. Effective limb length in HS and NHS walking. Effective limb length L′ was placed over the treadmill display, blocking time and speed data (m) is significantly longer during HS, heel-to-toe gait compared with NHS gaits from the subject. Subjects started the WTR protocol using a (N=14, F1,13 =459.8; *P<0.0001). Journal of Experimental Biology

3732 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610 low considering the length of the entire foot (from heel to toe in the 0.45 A sagittal plane) would not simply be added to total limb length in a 0.4 ′ true digitigrade gait. DC L was also significantly shorter in NHS 0.35 trials (see Fig. S1; −0.247±0.109 m, P<0.0001) when compared 0.3 with HS trials at preferred walking speeds. Absolute HS walking speeds were significantly faster compared 0.25 with NHS walking across self-selected speed categories 0.2 0.15 (F1,13=8.43; P=0.012), however, post hoc tests showed that the HS slow walking speeds were not significantly different (P=0.49). HS 0.1 NHS Fr values (using hip height) were also significantly higher ) 0.05 –1 s compared with NHS postures at any given self-selected speed 0 N

(Fig. 4A; F1,13=8.78; P=0.011), yet there was no significant 3 0 0.1 0.2 0.3 0.4 0.5 difference between HS and NHS Fr′ [calculated using plantigrade Fr ′ (cm adjusted ELL (L )] in self-selected speeds (Fig. 4B; F1,13=0.543, 0.45 B . COL

P=0.4744). There was no significant difference between DC HS and E 0.4 NHS Fr′ (see Fig. S2; slow, P=0.10; preferred, P=0.48; fast, 0.35 P=0.87). 0.3 0.25 Estimated cost of locomotion _ 0.2 Estimated cost of locomotion (ECOL; see Eqn 2) was increased by an average of 0.029±0.007 cm3 Ns−1 at all speeds by NHS walking 0.15 [Fig. 5A; χ2(1)=9.92, P=0.0016] when using Fr. However, foot 0.1 _ posture had no significant effect on ECOL when Fr′ was used to 0.05 2 adjust for effective limb length [Fig. 5B; χ (1)=1.26, P=0.2614]. 0 These results suggest the effects of foot posture on the energetics of 0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 walking are due in some part to the increased ELL associated with a FrЈ HS gait. E_ was not significantly different between HS and NHS _ COL Fig. 5. Estimated cost of locomotion (ECOL) before and after accounting _ 3 −1 footfalls after calculating limb length dynamically [see Fig. S3; for the effects of HS on L. (A) ECOL [Vmusc/tc (cm Ns )] differed significantly χ2(1)=0.19, P=0.6660]. before limb length was adjusted for a heel-striking gait [N=12, χ2(1)=20.56, P<0.0001]. (B) The estimated COL was not significantly different between foot χ2 ′ Walk-to-run transition postures [N=12, (1)=2.23, P=0.1353] when using Fr . NHS gait WTR transition speeds (m s−1)weresignificantly lower than HS gaits (P=0.0025), and therefore subjects transitioned the WTR transition (Fig. 6; HS=0.322±0.038, NHS=0.319±0.041 to running at a significantly higher Fr during HS walking P=0.43). Thus, the differences in WTR transition speed between HS (HS=0.426±0.055, NHS=0.365±0.045, P=0.0025). However, when and NHS walking appear to be due to the effects of foot posture on ′ ′ taking into account L , there were no significant differences in Fr at ELL. DC dimensionless Fr′ WTR transition speeds were not statistically different between HS and NHS (see Fig. S4; P=0.34).

Fr number Impact transient 0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 0.4 NHS walking reduced impact transients by an average of HS(S) 0.447±0.031 bodyweights compared with HS walking (Fig. 7; χ 2 NHS(S) 1 =98.79, P<0.0001). Similar to running (Lieberman et al., 2010), subjects displayed minimal IT values (Fig. 7) during NHS walking HS(P) NHS(P) * HS(F) 0.6 A B NHS(F) A * * 0.5

HS(SA) 0.4 NHS(SA) 0.3 HS(PA) NHS(PA) 0.2 HS(FA) 0.1 NHS(FA) number (WTR transition)

B Fr 0 HS NHS HS adj NHS adj Fig. 4. The effect of L′ on Froude number. (A) Fr numbers differed significantly between preferred and fast trials (N=14, F1,13=8.78, *P=0.011). (B) After adjustment using L′, there was no significant difference between HS Fig. 6. The effect of foot posture on walk-to-run (WTR) speed. (A) Froude and NHS trials (N=14, F1,13=0.543, P=0.4744). HS, heel-strike; NHS, non- number for hip height (L) WTR transition speed was significantly different heel-strike; S, slow; P, preferred; F, fast; SA, slow adjusted; PA, preferred between HS and NHS trials (N=14, *P=0.0025). (B) However, L′ adjusted WTR adjusted; FA, fast adjusted. Fr′ transition speeds were not significantly different (N=14, P=0.43). Journal of Experimental Biology

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1.6 While there are important benefits to using an HS gait, we also 1.4 HS found that NHS postures effectively reduce ITs during walking, similar to results of studies examining ITs in NHS running gaits 1.2 NHS (Lieberman et al., 2010). These results suggest that the evolution of 1 consistent HS walking in our hominin ancestors came with trade- 0.8 offs and that foot anatomy specific to our lineage (e.g. a robust 0.6 calcaneal tuberosity) may reflect the tolerance of consistently high 0.4 ITs (see Gebo, 1992; Latimer and Lovejoy, 1989). IT (body weights) IT 0.2 Study limitations 0 While our results support the notion that there are trade-offs between 0 0.05 0.1 0.15 0.2 0.25 0.3 energy cost and impact forces in HS and NHS walking, the FrЈ estimation of energy costs from the inverse dynamics analysis relies Fig. 7. Impact transients (ITs) in HS and NHS gaits. HS ITs (in multiples of on key assumptions that require further testing. As noted by Roberts body weight) were significantly higher at all speeds compared with NHS ITs et al. (1998b) when developing this method, the link between active χ 2 (N=12, 1 =98.79, P<0.0001). muscle volume and the metabolic costs of locomotion relies on the assumption that muscle force produced per unit of cross-sectional area (σ) remains constant across experimental conditions. Within an throughout the self-selected speeds (range, 0.00–0.37 individual, this assumption is upheld across experimental bodyweights). IT values in HS trials, however, displayed much conditions if muscles operate with similar relative shortening greater variation and increased with speed (Fig. 7; range, 0.23–1.43 velocities (v/vmax) and in similar regions of the muscle force-length bodyweights). curve. If these assumptions are violated, the same muscle might activate different amounts of volume to generate a given force under DISCUSSION different experimental conditions. In our study, it is possible that This study examined the effects of both plantigrady and HS on the changes in ankle and knee kinematics lead to muscle activation at human walking gait. By experimentally altering foot posture during different shortening velocities or different portions of the force– walking, we measured the effects of intra-individual limb length length curve, which would limit our ability to estimate the energy changes on walking mechanics (i.e. L versus L′ under different costs of walking between gaits with very different limb postures. conditions). A plantigrade foot and HS ground contact lengthens the Previous work has shown that comparisons between humans and effective limb (21.9±3.9% compared with NHS L′) by shifting the other mammals walking and running with different joint postures do COP anteriorly across the entire length of the foot throughout stance. not violate these assumptions. As described earlier, estimates of Our results suggest that HS walking plays an important role in active muscle volume seem to reflect the energy costs of both minimizing energetic costs during walking, which is aided by walking and running in the same individuals (see Biewener et al., lengthening ELL (L′). As hypothesized, energy and speed 2004; Ren et al., 2010). Thus, differences in joint angles during differences between HS and NHS walking lose significance once stance across speeds do not significantly affect the use of this model. L′ is used to calculate Fr′. Thus, if human HS and NHS walkers This method also accounts for energy cost differences within were two different organisms with limb lengths adjusted for COP individuals using fundamentally different gaits. For example, translation, we would conclude that their locomotor costs scale despite key difference in joint posture (Pontzer et al., 2014), appropriately with limb length regardless of foot morphology or between-gait differences in active muscle volume in chimpanzees speed. Additionally calculating L′ using data from across the step, walking bipedally and quadrupedally explain differences in both dynamically and using a two-point, touchdown and toe-off metabolic cost measured through oxygen consumption (Sockol method, shows that translation of the COP effectively lengthens the et al., 2007). Similarly, metabolic costs and active muscle volumes inverted pendulum strut. While both methods are valid, we suggest increased proportionally in humans walking with a flexed-knee and that for ease of use by future researchers, the two-point method of hip gait compared with humans walking with normal extended-limb calculating L′ is appropriate for most studies. bipedalism (Carey and Crompton, 2005; Foster et al., 2013). This Our data also support the importance of ELL (and therefore foot- ‘groucho’ gait is an entirely novel gait pattern with limb joints acting posture) in determining WTR transition speed. The reduction in at different levels of flexion during stance phase. Finally, Wright transition speed during NHS walking is well explained by the and Weyand (2001) compared active muscle volume and metabolic increased L′ in HS compared with NHS walking. Using L′, Fr′ at the costs in forwards and backwards running. The heel touches down WTR transition does not differ significantly between HS and NHS after the toes in backwards running, making it a novel gait, and yet walking, even though absolute transition speeds are statistically the increased metabolic costs were matched by the same percentage different. Not surprisingly, because of the importance of limb length increase in active muscle volume (Wright and Weyand, 2001). in calculation of Fr, the Fr′ at which subjects transitioned from Therefore, while we did not test the assumptions of the active walking to running calculated using L′ was lower than values from muscle volume model using direct measures of metabolic cost, we previous research (Hreljac et al., 2008; Kram et al., 1997; believe there is strong support for its use here, and this method Thorstensson and Roberthson, 1987). Increased ELL due to HS provides an important perspective on the potential energetic gaits reduced Fr′ at the WTR transition to 0.322±0.038, which is advantages of walking with a consistent HS. close to values found for the walk-to-trot transition for horses across a broad size range (Fr≈0.30–0.37) (Griffin et al., 2004). These Evolutionary implications of HS walking results raise an intriguing suggestion that one advantage of HS foot- Our results have important implications for the reconstruction of posture is an increase in range of available walking speeds, delaying morphology and locomotor performance in the fossil record. Since the transition to a running gait. apes use a variety of footfall patterns in both quadrupedal and Journal of Experimental Biology

3734 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610 bipedal gaits, we believe it is likely that our pre-bipedal ancestors traits may improve climbing performance while putting less stable also experienced variation in foot postures at touchdown, including foot and ankle joints at a higher risk of injury in the presence of large both human-like HS, initial contact with the heel and midfoot impact forces during HS walking. Our results suggest that retaining simultaneously, and NHS walking, as examined here. If true, the NHS postures as part of their footstrike repertoire may have allowed evolution of consistent HS walking occurred some time within the A. sediba to maintain climbing ability by reducing impact transients. hominin lineage, either with the earliest bipeds, or later in human Although reductions in foot length occurred with the evolution of evolution. By focusing on the two extreme foot postures described the genus Homo, possibly to improve endurance running for nonhuman apes (HS and NHS), we have highlighted the effects performance (Rolian et al., 2009), variation in foot length of COP translation during the stance phase on locomotor suggests the advantages of a long L′ may have persisted in some biomechanics. In doing so, we have shown that a shift to a species until relatively recently. For example, Homo floresiensis,a consistent HS, as we suspect occurred during early human small-bodied hominin living on the island of Flores (Morwood evolution, has advantages over plantigrade species that use gaits et al., 2004), possessed relatively long feet compared with other with more minimal COP translations. members of the genus Homo (Jungers et al., 2009a). The foot of H. Foot anatomy in early hominins suggests that the use of a floresiensis (LB1) is roughly 70% of the length of its femur (Jungers consistent HS may have been beneficial across much of human et al., 2009a), which is exceptional compared with modern human evolutionary history. While the feet of early bipeds lack derived foot lengths (54% of femur length) (White and Suwa, 1987). The features seen in the genus Homo that allow for effective endurance long foot of H. floresiensis (Jungers et al., 2009b) would increase L′ running, they may have been well adapted to HS walking (Bramble to ≈0.797 m, a ≈43.6% increase from hip height (L≈0.555 m). Our and Lieberman, 2004; Spoor et al., 1994). For example, the sample of modern humans produced an average L′ of 1.18±0.06 m relatively short toes, and therefore shorter feet, seen in modern (L=0.90±0.05 m) for comparison. humans are advantageous to endurance running because they reduce Finally, Homo neanderthalensis feet display a unique mix of plantar–flexor moments at the metatarso–phalangeal joints (Rolian short toes (Trinkaus and Hilton, 1996) and long calcaneal tubers et al., 2009) and probably evolved with the origins of the Homo (Miller and Gross, 1998; Raichlen et al., 2011; Schmitt, 1998; genus. Australopithecus, a hominin genus that preceded Homo, had Trinkaus, 1975, 1983). The inclusion of short, robust limbs relatively long feet, which Rolian et al. (2009) hypothesize would (Holliday, 1997; Trinkaus, 1981) suggests that Neanderthals were have detracted from running performance. Our results suggest that lackluster runners compared with modern humans, raising future relatively long feet in australopithecines may have led to improved research questions about Neanderthal L′ and the selective pressures walking performance through increased translation of the COP, and on walking/running. Thus, our results provide a novel view of foot therefore increased ELL. Thus, foot proportions in fossil hominins length in the evolution of human walking and allow us to generate may reflect competing selection pressures for walking and new, testable hypotheses for inter-specific variation in energy costs endurance running. of walking throughout the human lineage. This hypothesis requires a walking gait with consistent human- like HS in species with relatively long feet. The Laetoli footprints Conclusions (fossilized footprints found in volcanic ash at Laetoli, Tanzania) are This study shows that human NHS walking decreases the anterior perhaps the best indicator that, by at least 3.6 million years ago, translation of the COP along the foot, shortening ELL (L′). ancient hominins walked with an HS (Leakey, 1981; Leakey and Adopting a plantarflexed foot posture at touchdown forced subjects Hay, 1979; Raichlen et al., 2010). Most researchers believe these to walk at a slower absolute speed, yet did not change the footprints were made by Australopithecus afarensis, and while dynamically similar foot posture adjusted Fr′ or estimated COL. complete fossil feet are rare in the early hominin fossil record, Additionally, NHS gaits reduced absolute WTR transition speeds estimated foot lengths suggest that these early bipeds had relatively but not WTR Fr′ compared with HS walking. long feet compared with modern humans (Sellers et al., 2005). By A long rigid foot may have been important to early bipeds by combining estimated foot lengths with COPc (see Fig. 1) and hip increasing walking speed in species that lack adaptations for excursion data collected here, it is possible to predict how increased endurance running. Our results suggest that both HS gaits and a foot length would have altered L′ in these early bipeds. Based on relatively long rigid foot may have lengthened L′ in early bipeds, fossil limb lengths and estimates of foot length (Jungers, 1988; thereby increasing maximum walking speed without affecting Sellers et al., 2005; Wang et al., 2004), A. afarensis (AL 288-1) had locomotor costs. While this was likely true for striding taxa like A. an L′ of ≈0.725 m when using HS gaits, an increase of ≈40.4% afarensis, other early bipeds, such as A. sediba may have retained from L for this species (≈0.516 m). In our sample of modern NHS gaits as part of their variation in foot-landing postures to humans, calculations of L′ increased effective limb length by preserve an arboreal lifestyle, with reduced impact transients 32.6±3.3% compared with L. Thus, the relatively long feet of allowing for skeletal features of the feet best suited for climbing. A. afarensis led to a greater increase in L′ compared with modern Future work should focus on additional advantages NHS walking humans. confers in specific ecological conditions inhabited by species with While long feet may have improved walking performance for more mosaic foot morphology, such as A. sediba. A. afarensis, other early bipeds may have walked without using an Interestingly, as endurance running entered the repertoire of early HS. For example, Australopithecus sediba, a South African hominin Homo species, toes shortened to reduce large digit flexor forces living approximately 2 million years ago (Dirks et al., 2010), (Rolian et al., 2009). The relationship between toe length (and thus exhibits foot and ankle morphology suggestive of more ape-like foot foot length) and absolute walking speed may have been mitigated by postures (Desilva et al., 2012; Zipfel et al., 2011). These features the acquisition of an efficient running gait, reducing the pressure of include gracile calcaneal tubers, increased mid-foot mobility, maintaining fast absolute walking speeds. Foot length, therefore, medial plantar processes indicative of pedal grasping ability, and may be seen as an indicator of selection pressures on walking or an ability to invert the foot similar to extant great apes during running in the fossil record, and foot length and posture play an vertical climbing (Desilva et al., 2012; Zipfel et al., 2011). These integral role in the evolution of bipedal locomotion. Thus, changes Journal of Experimental Biology

3735 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610 in hominin foot length may directly reflect selection pressures on Hreljac, A., Limamura, R. T., Escamilla, R. F., Edwards, W. B. and MacLeod, T. locomotor speed and energy costs. (2008). The relationship between joint kinetic factors and the walk-run gait transition speed during human locomotion. J. Appl. Biomech. 24, 149-157. Jungers, W. L. (1988). Lucy’s length: stature reconstruction in Australopithecus Acknowledgements afarensis (A.L.288-1) with implications for other small-bodied hominids. We would like to thank Stacey Tecot, Ivy Pike, Adam Foster, and Lizzy Eadie for their Am. J. Phys. Anthropol. 76, 227-231. thoughtful comments and guidance. We also thank David Carrier and two Jungers, W. L., Harcourt-Smith, W. E. H., Wunderlich, R. E., Tocheri, M. W., anonymous reviewers for insightful suggestions on a prior version of this manuscript. Larson, S. G., Sutikna, T., Due, R. A. and Morwood, M. J. (2009a). The foot of Additionally, we would like to thank the University of Arizona Statistical Consulting Homo floresiensis. Nature 459, 81-84. services. Finally, we thank all of the subjects for their time and cooperation. Jungers, W. L., Larson, S. G., Harcourt-Smith, W., Morwood, M. J., Sutikna, T., Awe, R. D. and Djubiantono, T. (2009b). Descriptions of the lower limb skeleton Competing interests of Homo floresiensis. J. Hum. Evol. 57, 538-554. Kram, R. and Franz, J. (2012). Is barefoot running more economical? Int. J. Sports The authors declare no competing or financial interests. Med. 33, 249-249. Kram, R. and Taylor, C. R. (1990). Energetics of running: a new perspective. Nature Author contributions 346, 265-267. Conceptualization, J.T.W. and D.A.R.; Methodology, J.T.W. and D.A.R.; Kram, R., Domingo, A. and Ferris, D. P. (1997). 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